Biological Conservation xxx (xxxx) xxxx

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Biological Conservation

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Perspective Scientists' warning to humanity on insect extinctions ⁎ Pedro Cardosoa, , Philip S. Bartonb, Klaus Birkhoferc, Filipe Chichorroa, Charl Deacond, Thomas Fartmanne, Caroline S. Fukushimaa, René Gaigherd, Jan C. Habelf, Caspar A. Hallmanng, Matthew J. Hillh, Axel Hochkirchi,j, Mackenzie L. Kwakk, Stefano Mammolaa,l, Jorge Ari Noriegam, Alexander B. Orfingern,o, Fernando Pedrazap, James S. Pryked, Fabio O. Roqueq,r, Josef Setteles,t,u, John P. Simaikav,w, Nigel E. Storkx, Frank Suhlingy, Carlien Vorsterd, Michael J. Samwaysd a Laboratory for Integrative Biodiversity Research (LIBRe), Finnish Museum of Natural History (LUOMUS), PO17 (Pohjoinen Rautatiekatu 13), 00014, University of Helsinki, Finland b Fenner School of Environment & Society, Australian National University, Canberra, ACT 2601, Australia c Department of Ecology, Brandenburg University of Technology Cottbus-Senftenberg, Cottbus, Germany d Department of Conservation Ecology and Entomology, Stellenbosch University, South Africa e Department of Biodiversity and Landscape Ecology, Osnabrück University, Barbarastraße 11, D-49076 Osnabrück, Germany f Evolutionary Zoology, Department of Biosciences, University of Salzburg, Salzburg, Austria g Institute for Water and Wetland Research, Radboud University, Heijendaalseweg, 135-6525 AJ Nijmegen, the Netherlands h School of Applied Sciences, University of Huddersfield, Huddersfield HD1 3DH, UK i Trier Centre for Biodiversity Conservation, Department of Biogeography, Trier University, Universitätsring 15, D-54296 Trier, Germany j IUCN SSC Invertebrate Conservation Committee, Universitätsring 15, D-54296 Trier, Germany k Department of Biological Science, National University of Singapore, 16 Science Drive 4, 117558, Singapore l IRSA–Water Research Institute, National Research Council, Verbania, Italy m Laboratorio de Zoología y Ecología Acuática (LAZOEA), Universidad de los Andes, Bogotá, Colombia n Center for Water Resources, Florida A&M University, Tallahassee, FL 32307, USA o Department of Entomology and Nematology, University of Florida, Gainesville, FL 32611, USA p Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zürich, Switzerland q Bioscience Institute, Federal University of Mato Grosso do Sul, Cidade Universitária, s/n, 79060-300 Campo Grande, MS, Brazil r Centre for Tropical Environmental and Sustainability Science (TESS), James Cook University, Cairns, QLD 4878, Australia. s Helmholtz Centre for Environmental Research, UFZ, Department of Community Ecology, Theodor-Lieser-Str. 4, 06120 Halle, Germany t German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, 04103 Leipzig, Germany u Institute of Biological Sciences, University of the Philippines Los Baños, College, 4031, Laguna, Philippines v Department of Water Science and Engineering, IHE Delft, 2611 AX, the Netherlands w Department of Soil Science, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa x Environmental Futures Research Institute, School of Environment and Science, Griffith University, Nathan, QLD 4111, Australia y Institute of Geoecology, Department Landscape Ecology and Environmental Systems Analysis, Langer Kamp 19c, D-38106 Braunschweig, Germany

ARTICLE INFO ABSTRACT

Keywords: Here we build on the manifesto ‘World Scientists’ Warning to Humanity, issued by the Alliance of World Arthropods Scientists. As a group of conservation biologists deeply concerned about the decline of insect populations, we Biodiversity loss here review what we know about the drivers of insect extinctions, their consequences, and how extinctions can Centinelan extinctions negatively impact humanity. Drivers of extinction We are causing insect extinctions by driving habitat loss, degradation, and fragmentation, use of polluting and Ecosystem services harmful substances, the spread of invasive species, global climate change, direct overexploitation, and co-ex- Threatened species tinction of species dependent on other species. With insect extinctions, we lose much more than species. We lose abundance and biomass of insects, diversity across space and time with consequent homogenization, large parts of the tree of life, unique ecological functions and traits, and fundamental parts of extensive networks of biotic interactions. Such losses lead to the decline of key ecosystem services on which humanity depends. From pollination and decomposition, to being resources for new medicines, habitat quality indication and many others, insects provide essential and irreplaceable services. We appeal for urgent action to close key knowledge gaps and curb insect extinctions. An investment in research

⁎ Corresponding author at: Finnish Museum of Natural History (LUOMUS), PO17 (Pohjoinen Rautatiekatu 13), 00014, University of Helsinki, Finland. E-mail address: pedro.cardoso@helsinki.fi (P. Cardoso). https://doi.org/10.1016/j.biocon.2020.108426 Received 15 November 2019; Received in revised form 27 December 2019; Accepted 19 January 2020 0006-3207/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/).

Please cite this article as: Pedro Cardoso, et al., Biological Conservation, https://doi.org/10.1016/j.biocon.2020.108426 P. Cardoso, et al. Biological Conservation xxx (xxxx) xxxx

programs that generate local, regional and global strategies that counter this trend is essential. Solutions are available and implementable, but urgent action is needed now to match our intentions.

1. Introduction 2015). In total at least one million species are facing extinction in the coming decades, half of them being insects (IPBES, 2019). Insect extinctions, their drivers, and consequences have received It is not only their vast numbers, but the dependency of ecosystems increasing public attention in recent years. Media releases have caught and humanity on them, that makes the conservation of insect diversity the interest of the general public, and until recently, we were largely critical for future generations. A major challenge now and in the unaware that insects could be imperilled to such an extent, and that coming years is to maintain and enhance the beneficial contributions of their loss would have consequences for our own well-being. Fuelled by nature to all people. Insects are irreplaceable components in this declining numbers from specific regions (Hallmann et al., 2017, 2020; challenge, as are other invertebrates and biodiversity in general. Lister and Garcia, 2018; Powney et al., 2019; Seibold et al., 2019; and Here we build on the manifesto World Scientists' Warning to many other studies), concern over the fate of insects has gained traction Humanity, issued by the Union of Concerned Scientists (1992) and re- in the non-scientific realm. issued 25 years later by the Alliance of World Scientists (Ripple et al., Current estimates suggest that insects may number 5.5 million 2017). The latter warning was signed by over 15,000 scientists and species, with only one fifth of these named (Stork, 2018). The number claims that humans are “pushing Earth's ecosystems beyond their capacities of threatened and extinct insect species is woefully underestimated to support the web of life.” (https://www.scientistswarning.org/the- because of so many species being rare or undescribed. For example, the warning/). As a group of conservation biologists deeply concerned IUCN Red List (version 2019-2) only includes ca. 8400 species out of about the decline of insect populations worldwide, we here review what one million described, representing a possible 0.2% of all extant species we know about the drivers of insect extinctions, their consequences, (IUCN, 2019). However, it is likely that insect extinctions since the and how extinctions can negatively impact humanity. We end with an industrial era are around 5 to 10%, i.e. 250,000 to 500,000 species, appeal for urgent action to decrease our knowledge deficits and curb based on estimates of 7% extinctions for land snails (Régnier et al., insect extinctions.

Fig. 1. Drivers (in red) and consequences (in blue) of insect extinctions. Note that drivers often act synergistically or through indirect effects (e.g., climate change favours many invasive species and the loss of habitat). All these consequences contribute to the loss of ecosystem services essential for humans (see Table 1). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

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2. We are causing insect extinctions behaviour (Desneux et al., 2007). Many fertilizers (including organic and mineral fertilizers) widely Irrespective of the precise trends and their spatial distribution, used in agriculture, can affect insect populations indirectly, via impacts human activity is responsible for almost all current insect population on the composition or quality of plant resources, on structural habitat declines and extinctions. Yet, in order to act, we first need to identify properties or causing soil acidification, and through eutrophication and quantify the different ways we are acting upon them, recognizing (Fox, 2013; Villalobos-Jiménez et al., 2016). Effects of high-levels of that much is still to be understood, and more often than not, several fertilizer use can be positive for a few herbivorous insects in agroeco- factors contribute synergistically to decline or extinction (Fig. 1). systems (e.g., aphids; Kytö et al., 1996), but have negative effects on most insects (Kurze et al., 2018; Habel et al., 2019a). Also, the use of 2.1. Habitat loss and fragmentation anthelmintic substances (e.g. Ivermectin) in livestock systems has a negative impact on the abundance and richness of insects associated Habitat loss, degradation, and fragmentation are probably the most with dung decomposition (Verdú et al., 2018). relevant threats to biodiversity (Foley et al., 2005; Dirzo et al., 2014; Industrial pollution (including air pollution, chemicals from fac- Habel et al., 2019a). Globally, 50% of endemic species of plants and tories or mining operations, and heavy metals) also causes insect po- vertebrates are restricted to some 36 biodiversity hotspots covering just pulation declines (Zvereva and Kozlov, 2010). Similar to pesticides, 2.5% of the Earth's surface (Mittermeier et al., 2004) and arguably, sub-lethal negative effects on individuals, and biomagnification along these hotspots likely harbour similar percentages of endemic insect food chains, add further threats to insect populations (Gall et al., 2015). species (Stork and Habel, 2014). Recent modelling suggests that agro- Several economically important insect species (such as pollinators or economic pressure for land will reduce the currently very restricted natural enemies of pests) may be threatened by chronic exposure to natural intact vegetation by a further 50% by 2050 in one third of the pollutants (e.g., heavy metals), but community-wide effects are often world's hotspots (Habel et al., 2019b). Processes associated with de- not well understood (Skaldina and Sorvari, 2019). Freshwater in- forestation, agricultural expansion, and urbanization are the proximate vertebrates (including several insect taxa) are disproportionately af- drivers of loss of natural or semi-natural habitats and their insect as- fected by pollution, with over 41% of species on the IUCN Red List semblages across the world (Brook et al., 2003; Basset and Lamarre, threatened by water pollution (Darwall et al., 2012). Industrial dis- 2019; Habel et al., 2019c). Mining is particularly relevant for sub- charge, sewage, and agricultural and urban run-off as well as increased terranean species, which are often spatially restricted (Mammola et al., sediment deposition, all reduce freshwater habitat quality (Jones et al., 2019a). Freshwater habitats additionally suffer from river flow reg- 2012). ulation and damming (Dudgeon et al., 2006). Increased siltation in Light and noise pollution are becoming increasingly pervasive rivers and streams from agricultural runoff (Wood and Armitage, 1997; globally (Morley et al., 2014; Gaston, 2018; Owens and Lewis, 2018), and references therein), as well as flow regulation, degrade habitats of and gaining a better understanding of these novel impacts is critical. typical stream dwelling insect larvae (Jones et al., 2012). There is also a Nocturnal insects are especially vulnerable to changes in natural light/ significant loss of pond ecosystems largely due to agricultural land dark cycles. Light pollution interferes with insects that use natural light drainage and urban development (e.g., Boothby and Hull, 1997; Wood (from the moon or stars) as orientation cues for navigation and with et al., 2003). communication of insects that use bioluminescent signals, such as Habitat loss is often accompanied by habitat fragmentation, and fireflies. It desynchronizes activities triggered by natural light cycles, both lead to decreasing connectivity (Fischer and Lindenmayer, 2007; such as feeding and egg-laying, and causes temporal mismatches in Fletcher Jr. et al., 2018). However, depending on the mobility of the mutualistic interactions (Owens and Lewis, 2018). Noise pollution insect species and the degree of habitat fragmentation their relative greatly changes the acoustic landscape and interferes with acoustic importance varies. Insects with low mobility may survive in isolated communication of insects and their auditory surveillance of the en- populations (e.g., many flightless Orthoptera; Poniatowski and vironment, having significant fitness costs (Morley et al., 2014). Finally, Fartmann, 2010; Poniatowski et al., 2018). In contrast, many species the effects of electromagnetic pollution on insects and other life-forms, with a higher mobility – such as butterflies – usually form metapopu- including humans, are still very badly understood and deserve further lations (Hanski, 1999). They depend on a network of suitable habitat exploration (Thielens et al., 2018). patches of sufficient size and in spatial proximity (Eichel and Fartmann, 2008; Stuhldreher and Fartmann, 2014). However, in less fragmented 2.3. Invasive species landscapes – even among metapopulation species – habitat connectivity usually plays a minor role for patch occupancy. Here habitat quality is Invasive alien species (IAS) are anthropogenically introduced spe- the main driver of insect species occurrence (Krämer et al., 2012; cies to locations outside of their natural geographical range, which have Poniatowski et al., 2018; Münsch et al., 2019). In these times of global a demonstrable environmental, ecological, or socio-economic effect warming, habitat connectivity becomes increasingly important for all (Turbelin et al., 2017). Impacts may be direct (e.g., through predation, insect survival. This is because insect range shifts in response to climate competition, or disease vectoring) and/or indirect (e.g., through trophic change are often constrained by insufficient habitat connectivity in cascades, co-extinction of herbivore or parasitoid hosts). Species in- fragmented landscapes (Platts et al., 2019), and so lag behind the in- troductions may ultimately lead to local loss of native insects, with crease in temperature, even for mobile species (Devictor et al., 2012; those exhibiting narrow geographic distributions or specialist feeding Termaat et al., 2019). habits being most vulnerable (Wagner and Van Driesche, 2010). Direct competition by non-native species can drive local populations 2.2. Pollution towards extinction (Williamson and Griffiths, 1996; Sala et al., 2000; Havel et al., 2015). The degree of ecological overlap with the invasive Pesticides are key drivers of insect declines due to their intensive ladybird, Harmonia axyridis Pallas, 1773, was a main predictor for local use, as well as inappropriate risk assessment regulations (Brühl and extinctions of endemic ladybird fauna in Britain (Comont et al., 2014). Zaller, 2019). Pesticides impact insect populations via direct toxicity Invasive ants (e.g. the Argentine ant, Linepithema humile Mayr, 1868) and sub-lethal effects (mainly insecticides), and indirectly through ha- are perhaps the best example of IAS that challenge native insect fauna. bitat alteration (mainly herbicides). Bioaccumulation, due to chronic Due to their large numbers and generalist predatory behaviour, many exposure and biomagnification along food chains, pose significant ad- invasive ant species are primary threats to native insects (see Wagner ditional threats for insect populations (Hayes and Hansen, 2017) that and Van Driesche, 2010). The invasive amphipod Dikerogammarus vil- can have undetected harmful effects on insect physiology and losus (Sowinsky, 1894) kills significantly greater numbers of aquatic

3 P. Cardoso, et al. Biological Conservation xxx (xxxx) xxxx invertebrates than native amphipods, reducing invertebrate diversity includes unsustainable harvesting for use as pets and decoration (as and displacing native amphipod species (Dick et al., 2002; Rewicz et al., souvenirs and jewels), or as food resources and traditional medicine. 2014). Various insects are kept as pets, but they are especially popular in The high biomass and dense structure of invasive plants often has a Japan, where there are many illegally traded insects (Actman, 2019). major impact on insect communities (Strayer, 2010). The monotypic Ants maintained in commercial farms are probably the most common nature of invasive plants reduces the quantity and/or quality of food, pet insect in USA, but field crickets, praying mantids, antlions, cater- and leads to declines in essential resources for many insects (Severns pillars, and mealworms are also reported worldwide as household pets and Warren, 2008; Preston et al., 2012; Havel et al., 2015). Ad- (Smithsonian, 2019). ditionally, invasive plants can change matrix composition, adversely Ornamental insects as preserved decorations are also numerous, affecting insect host-parasitoid relationships (Cronin and Haynes, particularly regarding Lepidoptera and Coleoptera. Coloured wings and 2004). Invasive plants may also provide eco-evolutionary traps for elytra are used in jewellery, embroidery, and pottery (Prasad, 2007; native insects. Once an invader has outcompeted and displaced native Lokeshwari and Shantibala, 2010). In regions where market demand is hosts, it may act as a host that results in poor larval development, or high, ornamental insects are frequently imported in large numbers increased larval mortality (Sunny et al., 2015), leading to insect po- (Kameoka and Kiyono, 2003), which fuels an illegal export industry in pulation decline. areas where high-demand insects occur naturally (Kameoka and Invasive pathogens can also lead to native insect extinctions. Kiyono, 2003; New, 2005). Unsurprisingly, this demand for ornamental European strains of the fungal pathogen, Nosema bombi, are thought to insects has driven declines of sought-after species (Tournant et al., have resulted in the widespread collapse of North American bum- 2012; Huang, 2014). blebees (Cameron and Sadd, 2020). Furthermore, the introduced Entomophagy is another driver of overexploitation (Morris, 2004; bumblebee Bombus terrestris L., 1758 has caused the disappearance of Schabel, 2006). A worldwide inventory listed 2111 edible insect species the Patagonian bumblebee, B. dahlbomii Guérin-Méneville, 1835, across (Jongema, 2017), with number of collected individuals often exceeding much of its native range, either due to direct competition or the in- regeneration capacity (Cerritos, 2009). Wild populations are threatened troduction of pathogens to which the native species have no defences because collection practices became less selective and sustainable (Cameron and Sadd, 2020). (Illgner and Nel, 2000; Latham, 2003; Ramos-Elorduy, 2006), due to the dissipation of indigenous knowledge, which often includes the 2.4. Climate change sustainable use of edible insects and their habitat (Kenis et al., 2006). In many subsistence societies, insects provide protein supplements and Climate change poses threats to insects and the ecosystems they can constitute nearly a third of total protein intake during periods of depend on, whether terrestrial (Burrows et al., 2011), freshwater meat protein shortage (Dufour, 1987). (Woodward et al., 2010) or subterranean (Mammola et al., 2019b). The The overexploitation of insects as alternative medicine also poses a complexity of global climate change goes far beyond simply global risk. Demand for the hundreds of insect species that are used in such temperature increase (Walther et al., 2002; Ripple et al., 2019). It also practices is reportedly threatening insect biodiversity (Feng et al., leads to a variety of multifaceted ecological responses to environmental 2009). The commercial value of products based on medicinal insects changes, including shifts in species distribution ranges (Chen et al., comprises about US$100 million per year (Themis, 1997). 2011), phenological displacements (Forrest, 2016), novel interactions among previously isolated species (Krosby et al., 2015), extinctions 2.6. Co-extinction (Dirzo et al., 2014), and other unpredictable cascading effects at dif- ferent levels of ecosystem organisation (Peñuelas et al., 2013). Changes Specialisation has led to many insects becoming co-dependent, and in species phenology, distributions, reduction in body size, assemblage therefore, vulnerable to co-extinction (Dunn, 2005; Dunn et al., 2009). structure, and desynchronization of species-specific interactions are all Among these, numerous insect lineages have diversified with verte- linked to climate change (Scheffers et al., 2016). For example, some brates, either as parasites, epizoic mutualists, or commensal copro- British butterflies are emerging earlier than previously recorded, and in phages. At least 5000 louse (Phthiraptera) species have been described, some cases, before their nectar plants have flowered (Roy and Sparks, of which most (~4000) use avian hosts (Price et al., 2003; Smith et al., 2000). In addition, changes in functional feeding group diversity can be 2011). About 2500 flea species are recognised (Whiting et al., 2008) associated with changes in trophic interactions in food webs (Jourdan and > 6000 species of dung beetles are named (Schoolmeesters, 2019). et al., 2018). Numerous insect lineages have also diversified with invertebrate hosts. Aquatic insects are disproportionately affected by climate change, Insects of the order Strepsiptera (twisted-wing insects) are obligate due to the synergistic negative effects on freshwater ecosystems overall parasites of other insects, and > 600 species have been described, (Reid et al., 2019), and these insects having limited dispersal capacity, though they are dwarfed by the parasitic wasps, which are estimated to as well as them confronting barriers to their dispersal, particularly at include as many as 350,000 species (Gaston, 1991). Insects co-depen- higher elevations (Bush et al., 2013). There is a need for the develop- dent on plants are also extremely species rich, with gall-inducing insects ment and implementation of bioindicators, and dragonflies are emer- alone comprising as many as 211,000 species (Espírito-Santo and ging as taxonomic champions for aquatic ecosystems (Chovanec et al., Fernandes, 2007). Similarly, mycophagous insects are extremely di- 2015; Dutra and De Marco, 2015; Valente-Neto et al., 2016; Vorster verse and often co-dependent on a few fungal hosts (Wertheim et al., et al., 2020). Bush et al. (2013) dubbed dragonflies as ‘climate can- 2000). aries’, with dragonfly species assemblages being three times more Co-dependent insects are greatly at risk of extinction through their sensitive to climate variables than macroinvertebrate assemblages at specialised ecologies (Dunn, 2005; Dunn et al., 2009), even though family level. While there is evidence that water quality improvements examples of co-extinctions are rare (Colwell et al., 2012). Models sug- have offset recent climatic debt for stream macroinvertebrates gest that co-extinction events should be far more common (especially (Vaughan and Gotelli, 2019), this continued mitigation is not likely to among plant-dependent beetles and bird lice) than present records reverse or even halt trends in aquatic insect species declines. suggest (Koh et al., 2004a). This is either because of co-extinction events are poorly recorded, or due to unrecognised network resilience 2.5. Overexploitation owing to the ability of co-dependent insects being able to use many more species than previously assumed (Colwell et al., 2012). Though rarely considered, overexploitation may play a role in insect In the case of co-dependent insects, trophic cascades can be parti- decline for many groups. It primarily threatens free-living insects and cularly relevant (Strona and Bradshaw, 2018). Host species are lost due

4 P. Cardoso, et al. Biological Conservation xxx (xxxx) xxxx to habitat loss, as has been shown in Lepidoptera-host plant systems 2020). While insect conservation often target charismatic, rare, or (Pearse and Altermatt, 2013). A historical example of indirect effects of threatened species, the temporal and spatial trends of common and invasive species is the co-extinction of Christmas Island flea (Xenopsylla widespread species are often overlooked (Gaston, 2011). Numerical nesiotes Jordan & Rothschild, 1909), resulting from loss of the Christmas declines of common and widespread species impact the functioning of Island rat (Rattus macleari Thomas, 1887) due to the introduced black ecosystems more severely. As such, safeguarding ecosystem function rat (Rattus rattus L., 1758) (Kwak, 2018). There is evidence that decline may be suffering un-noticed, highlighting the need for insect mon- of mammals due to synergistic causes (climate change, habitat de- itoring and conservation beyond rare and threatened species. struction, hunting, etc.) lead to a pervasive co-decline of dung beetles at continental scales (Bogoni et al., 2019). The overexploitation of birds 3.2. Differences in space and time by the pet trade also threatens their dependent insects (Eaton et al., 2015). Insects and most arthropods are relatively small organisms that often occupy small microhabitats. As we move horizontally across a 3. We lose much more than species seemingly homogenous patch, small features, such as dead wood, rocks, or even a single tree can alter conditions, leading to replacement of All species, including insects, are valuable as unique combinations species and allowing higher richness to persist within the larger patch of evolutionary events, have innate value, and so require care and (Barton et al., 2009; Stagoll et al., 2012; Crous et al., 2013). Insects also conservation. Yet, as George Orwell put it in Animal Farm, “All animals partition themselves vertically, i.e. in a forest, we find soil, ground are equal, but some animals are more equal than others.”, with in- active, undergrowth, sub-canopy, and canopy species, all of which vertebrates being largely neglected in conservation efforts worldwide contribute to the hyper-diversity found in, for example, tropical rain- (Cardoso et al., 2011), the so-called “institutional vertebratism” forests (Stork et al., 2016). This way, insect assemblages tend to be (Leather, 2013). There is no reason why an insect species deserves composed of few very common and many rare species (Pachepsky et al., much less attention than a bird or mammal species. However, the im- 2001; McGill et al., 2007), leading to high levels of beta-diversity. Such portance of insect population declines and consequent extinctions goes high levels of species turnover can be difficult to monitor, as research way beyond loss of species and their intrinsic value. tends to describe overall arthropod richness and compositional changes Each species represents individuals, biomass, and functions being driven by the common species. Given their nature, it is much harder to lost, and therefore not available for other living beings. Each species quantify how rare species are responding to anthropogenic pressures contributes a unique piece to a complex living tapestry that changes in (van Schalkwyk et al., 2019). space and time. Each species represents an unrepeatable part of the Processes that homogenise natural systems decrease beta-diversity history of life. In turn, each species also interacts with others and their by removing rare species from the system. These pressures not only environment in distinctive ways, weaving a complex network that remove native species, but also simplify the system, reducing the di- sustains other species, including us (Fig. 1). versity of resources and biological interactions. Furthermore, they allow secondary invasions from ecologically dominant alien invasive 3.1. Abundance and biomass insects that outcompete or simply feed on the native fauna (Silverman and Brightwell, 2008; Roy et al., 2016; see section on invasive species). Hallmann et al. (2017) documented a loss of biomass of flying in- The edges of transformed areas, including linear structures such as sects of about 75% over 30 years. This negative trend occurred in roads, show large edge effects on beta-diversity. This suggests that the nature reserves in Germany. These results are a warning and stimulated presence of dominant species, either native or alien, reduce niche space an intense debate on the insect crisis. Also, in other parts of Germany, by outcompeting and effectively replacing rare species (Swart et al., declining abundances and biomass for a broader set of arthropods have 2019). been recorded (Seibold et al., 2019). Similar trends have been recorded Insects do not just partition themselves across space, but also time. for other parts of Europe. Large declines in abundance have also oc- Tropical rainforest cicadas and bush-crickets call during different times curred among UK butterflies and moths (Conrad et al., 2004, 2006; of the day and night or at different frequencies to avoid overlap Thomas et al., 2004; Shortall et al., 2009; Fox, 2013; Knowler et al., (Schmidt and Balakrishnan, 2015). At the other extreme are the peri- 2016; Storkey et al., 2016), dragonflies (Clausnitzer et al., 2009) and odic cicadas, which only emerge as adults every 13 or 17 years (prime carabid beetles (Brooks et al., 2012) in recent years. Negative trends are numbers to avoid frequent overlap). One of the major concerns with not restricted to Europe, but also occur in other parts of the world global climate change is how warmer temperatures might be interfering (Wagner, 2019). A global meta-analysis of insect abundances revealed a with arthropod phenology. For example, a population of the 17-year 45% decline across two-thirds of the taxa evaluated (Dirzo et al., 2014). cicada emerged after just 13 years in 2017 (Sheikh, 2017), which is Yet, the specific trend and strength of the decline or eventual increase is most likely due to the alteration of host tree cycles (Karban et al., not universal and changes according to taxon and region (Macgregor 2000). et al., 2019). Declines in insect abundance and biomass always precede species 3.3. Phylogenetic diversity extinctions, as this is a continuous, not binary, process. Although cri- tically dependent on the ecological role of the species, numerical loss in Phylogenetic diversity takes the evolutionary relationships between abundance, and by extension, biomass, reflect impairment of ecological taxa into account and reflects the evolutionary history of each species. function and provisioning of ecosystem services. For example, biomass Communities with identical taxonomic diversity may differ widely with is a measurement of the amount of energy flowing through trophic le- respect to their evolutionary past, depending on the time of divergence vels that insects represent. In turn, reduced abundance and biomass of species from their nearest common ancestor (Webb et al., 2002; affects ecosystem functionality and resilience, food web structure, and Graham and Fine, 2008). Studying the effects of species extinction on species interactions, such as plant-pollinators, population persistence, the phylogenetic tree of life is therefore imperative and provides a and many ecosystem services (Biesmeijer et al., 2006; Losey and complementary view to the loss of taxon diversity. Vaughan, 2006). Insects constitute a major branch of the tree of life, representing ca. These studies highlight numerical declines in abundance and bio- 480 million years of evolution (Misof et al., 2014). Preserving this mass at the landscape level, but also inform us that declines are not phylogenetic diversity is crucial to protect the evolutionary trajectories restricted to rare and endangered species only, but are also present for of the most successful taxonomic group on our planet. Understanding more abundant species (Habel and Schmitt, 2018; Hallmann et al., the phylogenetic relationships among and within species is crucial to

5 P. Cardoso, et al. Biological Conservation xxx (xxxx) xxxx avoid detrimental decisions in conservation management, such as ne- Threatened species are not a random subset of all the species. glecting populations with unique evolutionary histories (e.g., Price Threatened species tend to share biological traits that influence their et al., 2007), (re-)introducing non-native species or mis-adapted evo- extinction risk (Chichorro et al., 2019). In general, specialists in either lutionary lineages (Moritz, 1999), or outbreeding depression in captive habitat type or feeding regime, very small or very large species, and breeding projects (Witzenberger and Hochkirch, 2011). poor dispersers, are at highest risk. The decline of both habitat and Insects comprise many unique evolutionary lineages with some old resource specialist species has been documented for bees, beetles, relict groups, such as the Zoraptera, Mantophasmatodea, Mecoptera, or butterflies, dragonflies, and moths (e.g., Kotze and O'Hara, 2003; Koh Grylloblattodea. Among the latter, the Kosu Rock Crawler (Galloisiana et al., 2004b; Bartomeus et al., 2013). Species with narrower habitat kosuensis Namkung, 1974) is listed as Critically Endangered on the requirements have less ability to escape from multiple pressures. The IUCN Red List of Threatened Species (Chung et al., 2018). This species resource specialists depend not only on their effective population size, is only known from a single cave, whose temperature has risen by > but also on the availability of their resources. When organisms are 3 °C from increased tourism, reaching 1400 visitors per day. Another dependent on only one resource type, co-extinctions might also be more example is the Mauritian endemic grasshopper species Pyrgacris relictus likely to occur. Descamps, 1968, which belongs to a distinct family (Pyrgacrididae) Demise of both large and the very small species occurs among with only two species. This species, which only feeds on an endemic vertebrates (e.g., Ripple et al., 2017). There are two main reasons ex- palm species is Critically Endangered, and only known from a single plaining the demise of large species: 1) they usually require more re- locality, imperilled by construction of a golf course (Hugel, 2014). Loss sources and therefore exist at lower population densities than smaller of such distinct evolutionary branches of the tree of life is irreversible species, which in turn increases the risk of local extinction due to un- and leads to the loss of unique genetic diversity. predictable events; 2) they usually have traits related to slower life cycles and therefore respond slower to environmental change. On the 3.4. Functional diversity other hand, smaller species often decline in greater proportions than larger ones, due to their lower competitive ability (Powney et al., Functional diversity quantifies the components of biodiversity that 2015). However, small insects can be sensitive to fragmentation (Basset influence how an ecosystem operates or functions (Tilman et al., 2001) et al., 2015) and habitat loss (Jauker et al., 2013) due to poor dispersal and reflects the amount of biological functions or traits displayed by ability. species in given communities. Communities with completely different species composition may be characterized by low variation in func- 3.5. Ecological networks tional traits, with phylogenetically unrelated species replacing others with similar functional roles (Villéger et al., 2012). The functional di- Insects are crucial in structuring and maintaining communities, versity and role of insects in maintaining ecological processes are issues forming intricate networks that can influence species' coevolution of immense interest, and are particularly relevant to landscapes un- (Guimarães Jr. et al., 2017), coexistence (Bastolla et al., 2009), and dergoing anthropogenic change and biodiversity loss (Ng et al., 2018). community stability (Thébault and Fontaine, 2010; Rohr et al., 2014). This is because functional diversity provides a direct link between Insect extinctions not only reduce species diversity, but also simplify biodiversity and ecosystem processes. Moreover, loss of particular traits networks, and we may be losing interactions at a higher rate than can result in changes to key ecological processes promoted by insects, species (Tylianakis et al., 2008; Valiente-Banuet et al., 2015). The im- such as pollination (Saunders, 2018) and decomposition (Barton and plications of these changes will depend on the role a species plays in the Evans, 2017). network (Bascompte and Stouffer, 2009; Tylianakis et al., 2010). The

Table 1 Ecosystem services provided by insects. (Adapted from Samways, 2019)

Type of service Area Provision

Commercial Provisioning services Medicine New treatments Engineering Biomimetics Monitoring Monitoring of habitat quality Genetic resources New chemicals Ornaments Insect houses and deadstock Biocontrol Biocontrol agents Production Food and fibre Non-commercial Regulating services Climate Climate regulation Disease control Burial of dung or carcasses Erosion Limiting erosion Invasion resistance Controlling invasive species Herbivory Nutrient cycling Natural hazards Protection from hazards Pollination Reproduction of flowering plants Plant dispersal Seed dispersal of plants Water flow Regulating water movement Water treatment Purification by larvae Supporting services Nutrient cycling Through saprophagy/coprophagy Oxygen production Through interaction with plants Habitat creation Building mounts, nests, and others Soil formation Breakdown of plants, dung and carcasses Cultural services Cultural heritage Arts, myths, and stories Education Connecting with nature Knowledge systems Models for scientific research Recreation Nature tourism Sense of place Endemic species Spiritual values Views on nature

6 P. Cardoso, et al. Biological Conservation xxx (xxxx) xxxx more a species shapes a network, the more the architecture will change manipulative controlled experiments for several services (Noriega et al., if it goes extinct. Furthermore, species conferring network structure are 2018). Also, the few comprehensive studies available are focused on a most at risk of going extinct (Saavedra et al., 2011). Thus, we should few iconic groups or functions, such as bees and pollination (e.g., aim to preserve both species and their interactions (Tylianakis et al., Brittain et al., 2010), ground beetles and pest control (e.g., Roubinet 2010). et al., 2017), dung beetles and decomposition (e.g., Griffiths et al., In mutualistic networks, plants and insects weave nested relations 2016), or aquatic insects and energy flow (e.g., Macadam and Stockan, (Bascompte et al., 2003). This leads to specialists interacting with 2015). This critical shortfall must be addressed to conserve insect di- subsets of generalist interaction partners. Nested networks tend to mi- versity for our own survival. tigate random extinctions or the loss of specialists (Memmott et al., 2004). In this case, when species are lost, the structure remains. In 5. We need immediate action contrast, the extinction of generalists erodes the nested architecture. In this case, the loss of focal species makes the system more prone to co- The current extinction crisis is deeply worrisome. Yet, what we extinction cascades (Dunne et al., 2002). know is only the tip of the iceberg. We provide here numerous examples In antagonistic networks, species form intertwined subgroups, of the loss of species diversity and abundance, and their consequences, where inter-module interactions are rare (Olesen et al., 2007). Con- but these are some of the few well-documented examples. Most insect nectors and network hubs are important contributors to the modular species are undescribed (possibly as many as 80%; Stork, 2018), and structure, with beetles, flies, and small bees being the most common even for most of those with names we have no distributional or popu- connectors (Olesen et al., 2007). Alarmingly, some of these hub species lation trend data to record ongoing extinctions. Edward O. Wilson are currently at risk of extinction (Sirois-Delisle and Kerr, 2018). They (1992) called for a Linnean Renaissance to fully document and ap- not only benefit interaction partners, but also give cohesion to the en- preciate what is out there, and where, especially as many insect species tire community. Their disappearance may result in the fragmentation of are going extinct even before being described (Centinelan extinctions). networks into isolated modules (Bascompte and Stouffer, 2009; Despite the known threats and consequences of insect extinction, Tylianakis et al., 2010). This endangers communities by making them decision-makers and civil society are only now becoming aware of the more susceptible to perturbations (Olesen et al., 2007). scale of the problem. Conservation efforts have largely been focused on Interactions drive the coevolution of plants and insects (Bronstein charismatic megafauna, especially birds and mammals, with little et al., 2006). They can result in remarkable trait complementarity, as in thought on ecosystem connectivity (Cardoso et al., 2011; Donaldson the case of pollination or ant protection of plants (Bronstein et al., et al., 2016; Mammides, 2019). Even within insects, some taxa have 2006). Yet, in complex networks, indirect effects steer the evolution of been favoured, such as butterflies and, more recently, pollinators. traits (Guimarães Jr. et al., 2017). In species-rich networks, all members Legislation and agreements in the US (Endangered Species Act) and influence how traits evolve in the community. This means that extinc- Europe (Habitats Directive) clearly reflect such biases (Cardoso, 2012; tions will affect direct partners, and can reduce community-wide trait Leandro et al., 2017). Partly to blame for these biases is a lack of ca- integration. This could incapacitate entire communities from re- pacity and data, which, in the view of policymakers, leads to a lack of sponding to environmental change. funding, which in turn, feeds back into lack of capacity and data, in a continuous cycle. 4. We depend on insects Existing data on insect population trends and drivers have several problems (Cardoso and Leather, 2019), yet it is possible to minimize Insects contribute to the four main types of ecosystem services de- them by taking advantage of multiple datasets. Published data from fined by the Millennium Ecosystem Assessment (2003): i) provisioning scientific papers or grey literature, online sources, such as the Predicts services, ii) supporting services, iii) regulating services, and iv) cultural or Biotime databases, primary data from museum collections, as well as services (Noriega et al., 2018; Table 1). This animal group contributes multiple citizen science projects could be collated to better understand to the structure, fertility, and spatial dynamics of soil, and they are a richness, abundance, and composition data on insects across space and crucial element for maintaining biodiversity and food webs (Schowalter time. Knowledge gaps in space, habitat types, phylogeny, function, and et al., 2018). A large number of insects provide medical or industrial time could then be identified, and additional efforts made to embrace products (Ratcliffe et al., 2011), and globally, > 2000 insect species are them. Finally, any changes can really only be fully understood when consumed as food. Also, in agroecosystems, insects perform many dif- possible drivers are considered. Given the heterogeneity of data ferent functions, such as pollination, nutrient and energy cycling, pest sources, available predictor variables may vary across regions. Never- suppression, seed dispersal, and decomposition of organic matter, feces, theless, data on predictor values for the six main extinction drivers are and carrion (Schowalter et al., 2018). Today, the agricultural sector often available at global (e.g., Forest Watch; Hansen et al., 2013)orat already actively uses insect antagonists of pests (classical and aug- least regional levels. mentative biological control) or establishes habitat management prac- Given the multiple dimensions of insect diversity loss, any research, tices to promote insects as natural enemies of pests. In this context, as a monitoring and conservation initiative must minimize the phylogenetic, clear consequence, insect declines can negatively affect the main- functional, habitat, spatial, and temporal biases. Recently, Cardoso and tenance of food supply and put at risk human well-being. Leather (2019) proposed the development and global adoption of a All described services translate to monetary value. In an initial ap- standardized and optimized scheme that would allow comparisons proach, Costanza et al. (1997) estimated a global value of ecosystem across space and time with minimum investment per gain unit (Cardoso services at US$33 trillion annually. Later, ecosystem services provided et al., 2016). However, while a monitoring scheme is running, we know by insects were estimated to have a value of $57 billion per year in the enough to act immediately (Harvey et al., 2020). United States alone (Losey and Vaughan, 2006), and insect pollination Solutions include the removal of the root causes of the problem, the may have an economic value of $235–577 billion per year worldwide indirect drivers, as essential components of a transformative change of (IPBES, 2016). Additionally, the annual contribution of ecosystem our economy and society (IPBES, 2019). Many solutions are now services provided by dung beetles to the cattle industry can reach $380 available to support insect populations at sustainable levels, especially million in the USA (Losey and Vaughan, 2006) and £367 million in the through preserving and recovering natural habitats, eliminating dele- UK (Beynon et al., 2015). terious agricultural practices including harmful pesticides, im- However, there is little knowledge on the functional roles that in- plementing measures for avoiding or eliminating the negative impacts sects play in many ecosystems, with their values likely greatly under- of invasive species, taking aggressive steps to reduce greenhouse gas estimated. Absence of detailed information is related to lack of emissions, and curbing the deleterious effects of overexploitation of

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